Cent. Eur. J. Biol. • 6(2) • 2011 • 293-299
DOI: 10.2478/s11535-010-0119-9
Central European Journal of Biology
Seeing through the lizard’s trick:
do avian predators avoid autotomous tails?
Research Article
Bart Vervust*, Hans Van Loy, Raoul Van Damme
Laboratory for Functional Morphology, Department of Biology,
University of Antwerp,
B-2610 Wilrijk, Belgium
Received 24 June 2010; Accepted 16 November 2010
Abstract: Counter-adaptations of predators towards their prey are a far less investigated phenomenon in predator-prey interactions. Caudal
autotomy is generally considered an effective last-resort mechanism for evading predators. However, in victim-exploiter relationships,
the efficacy of a strategy will obviously depend on the antagonist’s ability to counter it. In the logic of the predator-prey arms race, one
would expect predators to develop attack strategies that minimize the chance of autotomy of the prey and damage on the predator.
We tested whether avian predators preferred grasping lizards by their head. We constructed plasticine models of the Italian wall
lizard (Podarcis sicula) and placed them in natural habitat of the species. Judging from counts of beak marks on the models, birds
preferentially attack the head and might also avoid the tail and limb regions. While a preference for the head might not necessarily
demonstrate tail and limb avoidance, this topic needs further exploration because it suggests that even unspecialised avian predators
may see through the lizard’s trick-of-the-tail. This result may have implications for our understanding of the evolution of this peculiar
defensive system and the loss or decreased tendency to shed the tail on island systems with the absence of terrestrial predators.
Keywords: Autotomy • Predation • Predatory • Prey arms race • Podarcis sicula
© Versita Sp. z o.o.
1. Introduction
There is increasing evidence that predators actually
evolve counter-adaptations in response to the defensive
adaptations of their prey species. Several cases are
known in which predators have evolved morphological
or physiological mechanisms, which allow them to
circumvent defensive tactics of particular prey. For
instance, Lake Tanganyika crabs Platytelphusa
armata have evolved robust chelae in response to
the unusually hard shells of their gastropod prey (e.g.
Spekia, Neothauma) prey [1] and North American
garter snakes (Thamnophis sirtalis) have become
resistant to the TTX toxins of Taricha newts [2]. More
commonly, animals adapt their predatory behaviour in
reaction to the defensive tactics employed by particular
prey species. Australian death adders (Acanthophis
praelongus) have learned to delay the consumption of
toxic toads (Bufo marinus) until the chemical defence
loses its potency [3]. Jumping spiders (Portia labiata)
make a detour and approach spitting spiders (Scytodes
pallidus) from the rear, opposite the end from which
the scytodid’s spit is fired [4]. Broad headed snakes
(Hoplocephalus bungaroides) may have evolved an
extreme sit-and-wait foraging habit because their prey
(velvet geckos, Oedura lesueurii) can detect chemicals
left behind by moving snakes [5].
Caudal autotomy, the ability to shed the tail, is
an intriguing defensive technique that has evolved
numerous times in a variety of prey animals [6-8].
Many aspects of lizard tail autotomy, including its
histological mechanisms, ecological significance, intraand interspecific variability, phylogenetic distribution
and evolutionary history have received considerable
attention (reviews in [8] and [9]).One facet that has not
been considered is the question of whether predators
may develop (within a lifetime or on an evolutionary
scale) behavioural mechanisms that lower the
effectiveness of tail autotomy as an escape tactic. The
high number of autotomized tails – compared to entire
* E-mail: [email protected]
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Seeing through the lizard’s trick: do avian predators avoid autotomous tails?
lizards – found in predator stomachs [10], indicate
that this is a highly effective antipredator strategy. On
the other hand, caudal autotomy carries a series of
important and potentially lifelong costs (for an overview
see [11]).
Here, we investigate the hypothesis that avian
predators will prefer grasping lizards by the head to
prevent both tail autotomy (inducing the likely escape
of the prey) and reducing the chance of damage to the
predator. That such behaviour would arise does not
seem improbable, as many predators typically attack
particular parts of their prey’s body. For instance, sharks,
lizards, birds, and mammals preferentially grasp and bite
their prey in the head or neck region [12-17]. While, this
inclination is generally thought to aid speeding up the
killing or swallowing process, or to serve in protection
against defensive biting, we examined which part of the
body of the lizard that an unspecialised avian predator
strikes at.
2. Experimental Procedures
2.1 Study system and species
This study was conducted on two small islets of the
Lastovo Nature reserve (Adriatic Sea, Croatia): Pod
Mrčaru (42°46,7N; 16°46,7E) and Pod Kopište (42°45,7N;
16°43,7E). Both islands are uninhabited and consist of
an elevated and more vegetated centre encircled by a
lower girdle of almost barren rocks. They contain dense
populations of the Italian wall lizard (Podarcis sicula),
a robust, diurnal, heliothermic lacertid lizard. There are
no predatory mammals on the islands. Most predation
on Podarcis sicula is likely due to yellow-legged gulls
(Larus michahellis) which visit and nest on the islands
in higher abundances than other species. Occasionally,
other possible bird predators visit the islands, including
Ravens (Corvus corax), Falcons (Falco eleonorae,
F. tinnunculus, F. peregrinus), common buzzards (Buteo
buteo), short-toed eagle (Circaetus gallicus), and
herons (Ardea cinerea, A. purpurea, Ardeola ralloides).
It should be noted that all of these occasional species
were only observed once of twice during the four-year
study on these islands. Additionally, gulls tend to chase
away more dangerous bird predators (e.g. crows and
falcons) and predation intensity increased near a gull
colony on Podarcis atrata [18]. The importance of gulls
as predators of lizards is debated (e.g. [19,20]).
We conducted a dietary investigation and therefore
collected random faecal pellets from around the gull’s
nests on the islands. The majority of regurgitates
contained food from only one foraging habitat. Our
dietary analyses showed that this species of gull feeds
on lizards. In 6% of the examined pellets (N=485) we
were able to find mandibles of lizards (B. Vervust,
unpublished). This high rate of occurrence suggests
a potentially important predatory role of this gull in
(insular) lizard populations. More detailed information
on the study system can be found in [21].
2.2 Model construction and experiment
Because direct observation of predation on lizards is
difficult, we used the marks left behind by predators
on plasticine models to make inferences about the
predators’ target. Plasticine and clay models have
demonstrated their utility in many previous studies of
predation on reptiles (e.g. [17,21-23]).
We produced 569 models of adult lizards by
pouring non-toxic plasticine (Aquasoft, Eberhard
Faber) into a flexible mould (pâte à modeller epoxy
superfine, Pascal Rosier) that was constructed using
a preserved museum specimen of Podarcis sicula,
the same species native to the islets. Because
males and females look the same from even a short
distance, we made use of a single morph only. The
models were painted to resemble the colours of live
animals according to the human visual system (nontoxic paint LIVOS) and checked the reflectance of the
models using a photospectrometer. A methodological
problem associated with the use of these models
is a possible different perception of the models by
avian predators [24]. Therefore we test reflectance
of models with a spectrophotometer; reflectance
spectra were obtained with a portable high-resolution
photospectrometer (model HR 2000, Ocean Optics,
Duiven, The Netherlands) to compare the colours of
the models (N=10) with those of real lizards (N=10).
This device detects reflection spectra of visible light
and UV-reflectance (200-1100 nm) with a resolution
of 1.5 nm. Visible and UV light is provided by a
deuterium-tungsten light source (DH 2000-Bal, Ocean
Optics, Duiven, The Netherlands), which generates
illumination for wavelengths from 200 to 1100 nm.
We made use of a coincident reflectance probe
(QR400-7-UV/VIS-BX, Ø 2.6 mm, Ocean Optics,
Duiven, The Netherlands) to take spectra of the
surface of each individual. In order to characterize
overall colouration, four reflectance spectra were taken
across the body of the animal or model (interparietal,
central mid dorsal spot and two lateral dorsal spots).
The spectra from these points were averaged by
calculating the mean reflectance intensity at the
876 increments from wavelengths 400–700 nm. The
difference between real and replica lizards was
clearly reflected in their reflectance spectra and the
spectral parameters. Real lizards had low reflectance
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B. Vervust et al.
percentages for all wavelengths relative to the replica
lizards (B. Vervust, unpublished data). The replica
lizards showed typical spectra with high reflectance of
550–680 nm.
We placed the plasticine models in rows (average
length: 65 m, range: 45-115 m), at approximately 2 m
intervals, putting each model in approximately the
same position as the last real lizard observed prior
to positioning the model (for details see [21]). Lizard
densities on these islands are exceptionally high [25].
Because of the structural complexity of the islands,
each model was not visible (from human eye view) from
the next, reducing the possible confounding effects of
pseudoreplication. Between 48 and 52 hours later,
we returned to the islands and noted the number and
location (head, trunk, tail, limbs) of beak marks on each
model. We considered a model as “attacked” when it
exhibited a clear beak mark. We discarded scars on the
models originating from territorial interactions with real
lizards and not from predatory attempts.
2.3 Statistical analysis
We assume that if attack location is solely a function
of body area, larger body parts will receive more beak
marks. Therefore, we determined the relative surface
areas of the head, trunk, tail and limbs by scanning
10 plasticine models using a HP Scanjet model 5590.
We then digitised the outlines and obtained the areas
(above as seen from a birds perspective) with the
TspDIG program (version 1.40, 01/17/2004; Rohlf J.F.,
Ecology and Evolution, SUNY, Stony Brook, 2007). We
considered four areas: head including neck (bordered by
the line between the anterior insertion of the upper arm),
trunk, tail (bordered by the line between the posterior
insertion of the thighs), and sum of the area of the foreand hind legs. We took the average of these values and
multiplied the percentage of the area with the observed
numbers of attack as the null hypothesis. When a model
exhibited several beak marks, the attack score was
divided between the body parts. For instance, for a model
with one beak mark on the head and one on the trunk,
we recorded 0.5 head and 0.5 trunk (i.e. each attacked
model was treated as a single observation). Calculation
Number of scars
1
2
3
4
5
6
of the standard errors for the percentage values was
performed using the equation: SE = sqrt (P(100-P)/n),
where P = the percentage and n = the sample size [26].
For determining whether our results might have been
confounded by constant sum constraints, we repeated
our analysis, leaving out the most attacked body region
(i.e., we tried to differentiate between preference and
avoidance). Statistical analyses were conducted with
SPSS (version 15.0).
3. Results
We recorded a total of 851 beak marks on 208 of the
569 lizard models (Table 1). 361 lizard models were
intact and undisturbed. The distribution of scars along
the model’s body length was not random (Χ23 =204.22,
P<0.001); a disproportionately higher number of
attacks were located on the models’ head and there
were relatively few on the extremities such as limbs and
tail (Figure 1). Rerunning the analysis but disregarding
the marks on the heads also indicated a significant
non-random distribution (Χ22=251.67; P<0.001). Again
the extremities and especially the tail region were less
often attacked than would be expected by chance.
Figure 1.
7
8
Expected (corrected for area of body part) and observed
percentages of beak marks, for each body part. Circles =
observed percentage, squares = expected percentages
with standard errors.
9
10
12
13
14
17
Head
96
26
18
16
5
6
3
2
0
0
0
0
0
0
Trunk
56
35
9
22
15
5
6
1
2
4
1
1
1
1
Limbs
17
9
6
1
1
1
1
0
0
0
0
0
0
0
Tail
17
8
5
2
4
1
1
0
0
0
0
0
0
0
Table 1.
Frequency of scars on the lizard models. Data are shown in the form of counts of scars on body part.
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Seeing through the lizard’s trick: do avian predators avoid autotomous tails?
4. Discussion
This study showed that even these unspecialised
avian predators might have a preference for attacking
the head of model lizards, resulting from an innate or
learning process. While a preference for the head might
not necessarily demonstrate tail avoidance, this topic
needs further exploration because it suggests that
even unspecialised avian predators (seagulls) may see
through the lizard’s trick-of-the-tail. This result may have
implications for our understanding of the evolution of
this peculiar defensive system. There are many reasons
why attacking the head would be preferred over the
body or tail that has nothing to do with tail autotomy.
Our results are in accordance with earlier studies,
involving a variety of predator and prey species. For
instance, loggerhead shrikes (Lanius ludovicianus)
attack their rodent prey mostly in the head and neck
region [27-29]. Grasshopper mice (Onychomys
torridus) kill horned lizards (Phrynosoma cornutum and
P. modestum) by chewing their cranium [14]. Opossums
(Didelphis albiventris) subjugate pitvipers (Bothrops
jararaca) by biting them in the head or neck region [30].
Grisons (Galictis spp.) handle snakes in a similar way
[13]. Burton’s legless lizards (Lialis burtonis) strike prey
skinks (Eulamprus heatwolei) preferentially in the head
region [31]. Even venomous snake species that release
prey after the first bite, typically target the head or thorax
region [32-34]. A methodological problem associated
with the use of models is a possible different perception
of the models by avian predators. We found a slightly
different reflectance of our models than values from real
lizards, and future studies should try to circumvent this
problem.
Additionally, we do not know the order of pecks, i.e.
which body-part is pecked at first. In nature, predators
likely have only one chance to capture and kill their prey
and do not have the opportunity for multiple strikes at
different parts of the same prey item’s body. If most
attacks on models are directed towards the head, then
these are probably also the first strikes the predator
made. In our analysis, we removed these first strikes,
which likely left us with mostly secondary, tertiary, etc.
strikes, which may be rare in natural situations. Also, it
stands to reason that if a predator strikes a plasticine
model once, then the probability that it strikes the same
model in a particular region for second and third strikes
may change depending on where the previous strike
occurred (i.e., learning). Thus, a given body region
does not have the same probability of being targeted
over time, so it is difficult to draw conclusions without
taking this into account. Finally, any potential effect of
prey movement (living organisms are not static), for
example movement of the tail, will make this body part
more conspicuous and possibly make birds more likely
to attack it. In a set-up similar to ours, Shepard (2007)
[17] found that models of four different lizard body
shapes were preferentially attacked in the head by both
lizard (Ameiva ameiva) and bird predators. Predators
may target the rostral end of prey because the head
and neck regions contain vital and vulnerable parts that
are relatively accessible [14,17,27,28]. In other cases,
seizing the head or neck of the prey may protect the
predator against dangerous defensive behaviour such
as retaliatory biting [30,31] or spitting [4]. An additional
advantage for predators preying on lizards and other
animals with autotomous tails might be that the head is
firmly secured to the trunk and situated far away from
the detachable end, so that the risk of ending up with but
a minor bit of the prey is limited.
However, the relatively low proportion of predatory
marks that we observed on our lizard models cannot be
explained solely in terms of a preference for the head
region. Tails also had proportionately fewer bite signs than
the trunk and limbs, suggesting that the bird predators
were actively avoiding the tail region. From the point of
the predator, this obviously makes sense – by targeting
the other regions of a lizard’s body, it can get around the
autotomy trick and benefit from the full energetic contents
of his catch. Although it is reasonable to assume that
selection should favour this kind of prudent predatory
behaviour, we have no idea whether the tail avoidance
in birds is adaptive in the sense that it arose as a genetic
counter-adaptation in response to the prey’s autotomous
abilities. Several studies have presented evidence that
different aspects of foraging behaviour can be innate (e.g.
[35-39]), so the hypothesis that bird brains are genetically
programmed to avoid grabbing lizard tails remains viable.
However it is also possible that birds (like herpetologists)
learn to avoid grasping tails in the course of their lifetimes.
A large number of studies have revealed the importance of
learning and prior experience on foraging proficiency in a
wide variety of predator species, ranging from arthropods
to humans (e.g. [40-43]). The ontogenetic flexibility of
foraging behaviour may vary considerably among even
closely related species (e.g. [42,44]), but theoretically
one would expect specialist foragers to have genetically
fixed foraging techniques, and generalists to have
flexible (learned) methods (cf. [42,45]). If so, because in
our study system none of the predator species can be
considered a lizard-hunting specialist, we suspect that
the tail avoidance behaviour is acquired through learning
or prior experience. It would be interesting to compare
the frequency of attacks on the tail of models exposed
to predators that differ in their prior experience with
lizards, and between generalist and specialist predators.
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While natural selection could have been acting for tail
avoidance to be hardwired in predators, it should be
noted that not all lizards autotomize their tails. Further,
because learning to avoid attacking the tail is not a costly
thing to learn, it seems unlikely that hard wiring such a
thing would be strongly selected for. In order to test the
idea of tail avoidance, future research could use models
of lizard species that the predator is familiar with that do
and do not autotomize their tail to investigate if there is a
difference in predator attacks on body regions.
Our results suggest that even generalist predators
may circumvent tail-autotomy. Why then, can lizards
still shed their tails? Shouldn’t natural selection push
lizards to abandon an unsuccessful anti-predation
strategy? Perhaps caudal autotomy is still valuable as
a defence technique against un-experienced predators.
Possibly, our methodology using immobile models also
underestimates the number of times that lizards will
be attacked on the tail, even by experienced hunters.
Behaviour of live lizards in the field (e.g. defensive and tail
displays) may lead to different patterns of attack to those
observed in this study. However, we never observed
such behaviour in our study species. In addition, the
costs of having an autotomous tail may not be great
[46,47], so the selection gradient working against tailshedding ability should also be rather shallow. From a
different perspective, the ability to shed the tail has been
lost (and has re-evolved) several times in squamate
evolutionary history, a fact usually attributed to shifts
in the cost-benefit balance of the strategy [8,48]. We
here suggest that changes in the ability of the predator
community to see through the lizards’ tail trick may be
a factor that has been overlooked in this respect. For
instance, for lizards hunted by a specialist predator
that has evolved the skill to avoid the treacherous tail,
autotomy has little selective advantage.
In our study system, the proportion of lizards showing
tail autotomy differed considerably. We found a significant
different degree of autotomy frequency, ranging from
25.5% in the Pod Mrčaru population up to 41% in de Pod
Kopište population [25]. This is in accordance with the
suspected difference in predation pressure [21].
We also do not know the frequency of gull’s attacks
either from the ground or from aerial attacks. But
unquantified observations suggest that gulls attacked our
models from the air. The lizards of our study system live
on islands with limited predators. Several authors found
that autotomy varies with predation risk [49]. If future
research on the interaction between visually oriented
predators (birds) shows a clear avoidance of the tail
region, the outcome of this result does not hold for other
(chemical oriented) predators such as snakes and rats.
The review of Bateman and Fleming (2009) [9] suggested
that knowledge of how different predator taxa attack
lizards will inform us about autotomy frequency pattern
differences between populations. Avian predators might
not be a selective force resulting in the maintenance of
autotomy, seeing as they will come directly from above
and are also often much larger than their prey. This is
supported by Cooper et al. (2004) [49] who found loss of
autotomy in lacertids on islands where the only predators
were gulls and kestrels. Most predators are well aware
of where the head and eyes of very different taxa are
situated, which influences attack and defence/vigilance
behaviour. Attacking the head induces an immediate kill
and it incapacitates the area most likely to inflict damage
on the predator. This hypothesis seems more probable
and logical and seems considerably stronger than that of
autotomy, especially given the prevalence of this type of
attack behaviour among predators of all trophic levels, as
mentioned above, attacking both autotomising and nonautotomising prey. We feel that this intriguing possibility
deserves further study.
Acknowledgements
We appreciated the help and company of Jan Scholliers
in the field. This study is part of larger projects supported
by the FWO – Flanders (project nr. G.0111.06) and the
Research Fund of the Republic of Croatia (project nr.
183007). Research was carried out under research
permit UP/I 612-07/04-33/267 issued by the Croatian
Ministry of Culture.
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